THE HYPOTHESIS OF COEVOLUTIONARY ALTERNATION WITH ESCALATION: A PRELIMINARY TEST USING NATICID GASTROPODS AND THEIR BIVALVE PREY

The hypothesis of coevolutionary alternation with escalation attempts to explain how levels of defense and counterdefense in multispecific interactions evolve (Thompson, 2005). Selection is hypothesized to favor consumers (predators, grazers, parasites) that preferentially select among multiple species those prey with the lowest levels of defense, which results in evolution of improved defenses in those prey. Simultaneously selection favors the loss of defenses in unattacked prey species. Evolutionary changes in relative levels of prey defense should result in selection favoring predators that prefer prey species that are currently least defended. Because variation in selection inevitably occurs in any widespread interaction, prey defenses and predator preferences should vary geographically.

The naticid gastropod predator-prey system is ideal to test this hypothesis in the fossil record due to the wealth of data on morphological defenses of prey and on predator preferences indicated by naticid drilling frequencies (DF). In a preliminary test of the hypothesis, we examined prey defenses and predator preferences in the Miocene Calvert Formation of Maryland. Two different localities at a single stratigraphic level yielded the same preference rankings for three common prey: Marvacrassatella melina DF > Astarte cuneiformis DF > Dallarca subrostrata DF. Dallarca had both the lowest cost-benefit ratios (= least defended) and the lowest DF. Levels of defense for a given taxon varied little geographically.

Our preliminary test does not support the hypothesis of coevolutionary alternation with escalation. The highest DF did not correspond to the least defended (thinnest) prey species. Prey defenses and preference rankings by the predator also did not vary geographically as predicted. Our results may reflect the fact that the hypothesis of coevolutionary alternation focuses on the evolution of local, highly specialized adaptations, while in our study adaptations forged by selection due to enemies are more general. Many adaptations, including thick shells, are general responses to classes of enemies. Although limited at present by geographic scope, our data challenge whether this hypothesis can explain more complex evolutionary patterns of defenses and counterdefenses found in the fossil record.